Effectiveness of Native Solitary Bees in Seed Production of Sesame (Sesamum indicum L.)

Sesame (Sesamum indicum L.) is a member of Pedaliacea family (Ranjithkumar and Kumar, 2020) and is among the top ten traditional oil seed crops grown in Pakistan (Hameed and Azeem, 2017). Pakistan is facing extreme deficit in edible oil (Hussain et al., 2017) and is importing 88% of edible oil (3.13 million ton) annually (Mustafa, 2019). Oil extracted from sesame contains high nutritional value and stability against oxidative rancidity (Borchani et al., 2010). Moreover, sesame seeds contain 50% oil content, which is the main reason behind its cultivation (Kurt, 2018). Furthermore, it is valuable in food, chemical industries and in the field of medicine (Blal, 2013; Elleuch et al., 2007). Nutritionally, sesame seeds contain 44–57% oil, 13–14% carbohydrates, and 18–25% protein (Borchani et al., 2010). Sesame covers about 7.8 million hectare of the total world crop area (FAOSTAT, 2012). According to Pakistan Bureau of Statistic during 2017-18, almost thirty thousand tons of sesame seeds were produced in an area of 176 thousand acres in Pakistan.

Pollinators play a great role in global food security. About 75% of commonly grown crops all over the world depend on the pollinators for their reproduction (Klein et al., 2007). Animal pollination, especially by insects contributes about 35% of global food production and about 22.6% pollination of crops depend on bees (Aizen et al., 2009). Moreover, pollinators also contribute in improving quality of fruit in term of increasing nutritional value of the crops used for human diet (Wietzke et al., 2018; van der Sluijs and Vaage, 2016). Wild bees are significant pollinators of crops and substantially contribute to food production (Kleijn et al., 2015; Mallinger and Gratton, 2015). The increasing attention towards wild bees as alternative pollinators shows wild bees are more efficient pollinators as compare to honeybees. Wild bees contribute significantly in crop pollination by providing 150 billion dollars worth pollination services all over the globe (Gallai et al., 2009).

Sesame crop consider to be auto-pollinated but flower encourages cross-pollination (Stein et al., 2017; Andrade et al., 2014). Qualitative and quantitative characters of sesame enhance with open-pollination as compared to control one (Blal et al., 2013). However, pollination by wild bees and the honey bees increase the yield up to 59% in sesame crop (Stein et al., 2017). Honeybees also play a significant role in the cross pollination of sesame (Parmar et al., 2017). Some previous studies have been reported that non-Apis bees (Xylocopa sp. and Ceratina tarsata) and honey bees (A. mellifera, A. cerana) were the most abundant pollinators in sesame crop (Kamel et al., 2013).

The purpose of our study is to identify local pollinators of sesame, their abundance and diversity as well as their pollination efficiency. This study evaluates the individual pollinator efficiency in terms of single visits, visit duration and visitation rate. By identifying the effective native insect, we can increase the seed yield and quality of sesame by conserving these native insect pollinators.

Study was conducted at the research farm of MNS- University of Agriculture Multan, Pakistan. The experimental crop was sesame (Sesamum indicum L.) branched stem variety that was sown for 2 growing seasons 2019-2020, on an area of 0.5 acres. The experimental plot and sowing of sesame were homogeneously designed to avoid any variation that could affect the analytical comparisons of experiment. After sowing, manual removing of weed, management of pest and soil management (fertiliser and irrigation application) were done by standard means. Sesame field was surrounded by sunflower and cotton in south during both the years. The study area has subtropical climate with harsh conditions in hot summers and cold winters with the average monthly temperature of 35oC to 40oC.

To check the abundance and diversity of different insect pollinators, we selected 15 plants randomly. The insect visitors were recorded by observing each plant for 1 minutes and number of pollinators visiting flowers were observed and counted. Observations were made at 0700, 1000, 1300 and 1600 hours. Insects’ samples were collected for later taxonomic identification (Vockeroth, 1969; Michener, 2000).

Foraging behavior of different insect pollinators were recorded in terms of visit duration (time spent during contact with reproductive parts of the flower) and visitation rate (number of flower visited per minute). Weekly observation was done.

To check the effectiveness of insects in sesame crop in terms of pod formation and seed formation, we selected 20 plants each for no insect visit (caged treatment) and free insect visits (open pollination treatment). Thereafter, pods were harvested and their different parameters (i.e., capsule length, capsule weight, number of seed per capsule and seed weight per capsule) were recorded for comparison (Mahmoud, 2012).

To confirm the insect efficacy in relation to single visit, we caged the flower buds with muslin cloth before these opened. These buds were un-caged during the

Table 1: Insect species visiting Sesame indicum along with their abundance.

Table 2: Pollination effectiveness of pollinators in terms of visitation rates and stay time.

peak activity period of insect pollinators. After single visit by a specific pollinator species, we re-caged the flower to avoid further visits. Different seed yield parameters (Capsule length, Capsule weight, no. of seed per capsule and seed weight per capsule) were measured to assess the pollination success of individual insect (Ali et al., 2011).

The data for visitation rate, visit duration, capsule length, capsule weight, no. of seed per capsule and seed weight per capsule were subjected to statistical analysis (ANOVA). Moreover, statistical analysis was accomplished using the computer software XLSTAT (2011). There means were compared by using Fisher LSD test at p=0.05.

During the two growing seasons of sesame, eight bee and two syrphid fly species visited the sesame flowers. Overall, solitary and social bees comprised of 59% and 41% of total abundance, respectively. Among solitory bees, Amegilla sp. (606 individuals) was the most abundant followed by N. oxybeloides (304 individuals) while Xylocopa sp. (57 individuals) was the least abundant. Furthermore, among social bees, A. dorsata (751 individuals) was abundant followed by A. florea (304 individuals). Among syrphidae, Eristalinus aeneus (135 individuals) was the abundant followed by Ischiodon scutellaris (38 individuals) (Table 1).

In terms of visit duration, A. dorsata spent highest time per flower (20.83 ± 1.32 sec) followed by N. oxybeloides (13.01 ± 1.17 sec) while A. florea spent least time on a flower of sesame (4.95 ± 0.22 sec). Contrarily, visitation rate per minute was highest for Amegilla sp. followed by N. oxybeloides and A. dorsata (Table 2).

The number of seeds per capsule (F=13.8, df=5.0, p\0.0001) and seed weight per capsule (F=37.2, df=5.0, p\0.0001) were significantly different among the five pollinators (Table 3). Among all pollinators, Amegilla sp. produce more seeds per capsule and high seed weight in a single visit followed by A. dorsata, N. oxybeloides while least seed were produced by single visit of E. aeneus. Furthermore, there were statistical differences among capsule weights (F=7.9, df=5.0, p\0.0001) after single visits of pollinators (Table 3). Maximum capsule weights were observed after visit of Amegilla sp. followed by A. dorsata, N. oxybeloides and A. florea. Maximum capsule lengths (F=214, df=5.0, p\0.0001) were observed after visits of Amegilla sp. followed by A. dorsata (Table 3). The open pollinated flowers had better capsule weight and capsule length than the caged flowers.

Table 3: Comparison of reproductive success parameters of Sesame crop.

In our study, the proportional abundance of wild bees (57%) was greater than honey bees (43%). Contrarily, studies show in sesame crop proportional abundance of honey bees was higher than wild bee (Das and Jha, 2020; Mahfouz et al., 2012). However, Auguste et al. (2018) stated that there is equal proportional abundance of honey bees and wild bees in sesame. Similar trend was observed globally in other oilseed crops, the proportional abundance of wild bee (60%) was higher than honey bee (40%) in canola (Fuzaro et al., 2019) and in sunflower proportion of wild bees was 70% and honey bees 30% (Silva et al., 2018). In contrast honey bees were most abundant followed by wild bees and syrphid flies in mustard crop (Kunjwal et al., 2014) and in sunflower (Chambó et al., 2011). However, In Pakistan, the trend was same in some oilseed crops where proportional abundance of honey bees was higher than wild bees in mustard (Shakeel et al., 2018), in canola (Ali et al., 2011; Akhtar et al., 2018) and in sunflower (Ali et al., 2015).

Visitation rate is an important parameter for evaluating the efficiency of native insect pollinators (Albano et al., 2009). In our study, visitation rate of wild bees was higher than honey bees. Amegilla bee has higher visitation rate followed by N. oxybeloides while A. florea has lowest visitation rate. In other oil seed crop wild bees have higher visitation rate than honey bees in rapeseed (Stanley et al., 2013) and in canola (Ali et al., 2011). In Pakistan, other than oil seed crops wild bees have high visitation rate than honey bees in Capparis aphylla (Latif et al., 2016), cucurbits (Ali, 2017), Ocimum basilicum (Latif et al., 2017) and in Albizia lebbeck (Latif et al., 2018).

Visit duration is also an important parameter to asses efficiency of pollinators (Martinez and Wyatt, 2003). In our study, A. florea has highest visit duration while Amegilla bee and N. oxybeloides has lower visit duration. However, similar results were observed in canola where honey bee stays more longer on canola flower followed by wild bee (Ali et al., 2011). Contrarily, in sunflower visit duration of wild bee is greater than honeybee. The variation in visit duration could be assessed in terms of proportion of nectar present in flower (Ahmad et al., 2018).

The effectiveness of native pollinators can be asses as the proportion of seed formed in the result of single visit (Barrios et al., 2016). In our studies single visit by wild bee Amegilla cause higher yield in term of capsule length, capsule weight, number of seed followed by N. oxybeloides while E. aeneus produce the least yield. Previous studies shows that visits of wild pollinators increase fruit set, even in the presence of managed bees which suggests that the wild pollinators contribution is unique and additive to that of managed bees (Carvalheiro et al., 2010). Different studies have been reported in other oilseed crop, single visit by wild bee Halictus sp. in canola (Ali et al., 2011), Andrina in sunflower (Mallinger et al., 2018) Andrena spp. in rapeseed (Phillips et al., 2018) produce significantly more seed then honey bees. Moreover, In Pakistan wild bee Amegilla is efficient pollinator of C. aphylla (Latif et al., 2016) while N. oxybeloides is effective pollinators of cucurbit (Ali, 2017) and both are effective pollinators of A. lebbeck (Latif et al., 2018) which increase seed yield in single visit. Previous studies show in agro-ecosystems wild bees provide better pollination than managed bees (Rader et al., 2012).

Our findings describe the potential of solitary bees and wild honey bees in sesame seed production. Therefore, conserving these effective native insect pollinators will lead to better seed yield and resultantly higher oil yield. For conservation of solitary bees, some areas should be left un-ploughed that will provide soil nesting bees better place to breed (Sajjad et al., 2008). Nest sites i.e., bee hotels, tree trunk should be provided at small scales in addition to maintaining abundant foraging resources in the landscape (Kline and Joshe, 2020; Everaars, 2012). Future research should focus on the effectiveness of these native solitary and wild honey bee species for other crops grown in South Punjab, Pakistan.

Best of our knowledge no previous work has been done on single visit seed set efficacy of insect pollinators in sesame. Diversity of native efficient insect pollinators has been described first time for sesame seed production in South Punjab, Pakistan.

Mudssar Ali, Muhammad Awais Ahmad and Asif Sajjad: Conceived and designed the experiments.

Mudssar Ali and Muhammad Awais Ahmad: Performed the experiments, analyzed the data and Wrote the paper.

Mudssar Ali, Muhammad Awais Ahmad, Asif Sajjad and Shafqat Saeed: Contributed reagents/ materials/ analysis tools.

All the authors commented on previous versions of the manuscript.

There is no conflict of interests regarding the publication of this article.